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Innovations in parasitic weeds management in legumecrops. A review

Rubiales, Fernández-Aparicio

To cite this version:Rubiales, Fernández-Aparicio. Innovations in parasitic weeds management in legume crops. A review.Agronomy for Sustainable Development, Springer Verlag/EDP Sciences/INRA, 2012, 32 (2), pp.433-449. �10.1007/s13593-011-0045-x�. �hal-00930517�

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REVIEW ARTICLE

Innovations in parasitic weeds management in legume crops.A review

Diego Rubiales & Mónica Fernández-Aparicio

Accepted: 16 April 2011 /Published online: 4 August 2011# INRA and Springer Science+Business Media B.V. 2011

Abstract Parasitic weeds decrease severely the productionof major grain and forage legumes. The most economicallydamaging weeds for temperate legumes are broomrapes, inparticular Orobanche crenata. Broomrape species such asOrobanche foetida, Orobanche minor, and Phelipancheaegyptiaca can also induce high local damage. Otherparasitic weeds such as Striga gesnerioides and Alectravogelii decrease yield of legume crops throughout semi-aridareas of sub-Saharan Africa. Dodders such as Cuscutacampestris can be damaging for some crops. Here, wereview methods to control parasitic weeds. Preventing themovement of weed seeds into uninfested areas is a crucialcomponent of control. Once a field is infested with parasiticweeds, controlling its seed production is very difficult. Theonly effective way to cope with parasitic weeds is to applyan integrated approach. Seedbank demise can be achievedby fumigation and solarization. However, this method is noteconomically feasible for low-value and low-input legumecrops. A number of cultural practices including delayedsowing, hand weeding, no-tillage, nitrogen fertilization,intercropping, or rotations can contribute to seed bankdemise. Other strategies such as suicidal germination,activation of systemic acquired resistance, biocontrol ortarget site herbicide resistance are promising solutions that arebeing explored but are not yet ready for direct application. The

only methods currently available to farmers are the use ofresistant varieties and chemical control, although both havetheir limitations. Chemical control with systemic herbicidessuch as glyphosate or imidazolinones at low rates is possible.Advances in modeling and the availability of new technolo-gies allow the development of precision agriculture or site-specific farming. The most economical and environmentallyfriendly control option is the use of resistant crop varieties;however, breeding for resistance is a difficult task consideringthe scarce and complex nature of resistance in most crops.These strategies for parasitic weed management in legumecrops will be presented and critically discussed.

Keywords Parasitic weeds . Control . Breeding .

Intercropping . Germination . Biological control . Chemicalcontrol . Alectra .Cuscuta .Orobanche . Striga .

Broomrape . Dodder

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32. Cultural practises . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43. Chemical control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8

3.1 Herbicides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83.2. Suicidal germination . . . . . . . . . . . . . . . . . . . . . .123.3. Activators of systemic acquired resistance . . . . .13

4. Biological control . . . . . . . . . . . . . . . . . . . . . . . . . . . .145. Resistance breeding . . . . . . . . . . . . . . . . . . . . . . . . . . 16

5.1 Breeding for resistance to the parasites . . . . . . . .165.2 Pathogenic variation . . . . . . . . . . . . . . . . . . . . . . 185.3 Resistance mechanisms . . . . . . . . . . . . . . . . . . . .195.4 Potential use of molecular markers and biotechnolo-

gies in resistance breeding . . . . . . . . . . . . . . . . . . . 21

D. Rubiales (*) :M. Fernández-AparicioInstitute for Sustainable Agriculture, CSIC,Apdo. 4084,14080 Córdoba, Spaine-mail: [email protected]

M. Fernández-AparicioDepartment of Plant Pathology, Physiology, and Weed Science,Virginia Tech,Blacksburg, VA 24061, USA

Agron. Sustain. Dev. (2012) 32:433–449DOI 10.1007/s13593-011-0045-x

5.5 Lessons to learn from model legumes . . . . . . . . 235.6 Breeding for resistance to the herbicides . . . . . .. 25

6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26

1 Introduction

About 4,000 flowering plant species have adapted toparasitize other plants. Unfortunately for farmers, a smallnumber of these species have become weeds, posing severeconstraints to major crops including grain and foragelegumes (Rubiales and Heide-Jørgensen 2011). The mosteconomically damaging on legumes are the broomrapes(Orobanche and Phelipanche). Other parasitic weeds suchas Striga gesnerioides (Willd.) Vatke, Alectra vogueliiBenth. and the dodders (Cuscuta spp.) can be alsodamaging on some legumes (Joel et al. 2007; Parker2009) (Fig. 1).

Orobanche crenata Forsk. (crenate broomrape) is animportant pest of most grain and forage legumes beingwidely distributed in the Mediterranean basin and MiddleEast (Rubiales et al. 2009b) (Fig. 2). Orobanche foetidaPoir. in contrast is of importance only on faba bean (Viciafaba L.) in Beja region of Tunisia (Kharrat et al. 1992)although it has recently also been found in Moroccoinfecting common vetch (Vicia sativa L.) (Rubiales et al.2005b). Orobanche minor Sm. is widely distributed but ofeconomic importance on clover (Trifolium sp.) only(Eizenberg et al. 2005). Phelipanche aegyptiaca (Pers.)Pomel (syn. Orobanche aegyptiaca Pers.) is an importantpest of legumes but also of many vegetable crops in theMiddle East and Asia (Parker 2009). S. gesnerioides andAlectra vogelii cause considerable yield reduction of grainlegume crops, particularly cowpea (Vigna unguiculata (L.)Walp), throughout semi-arid areas of sub-Saharan Africa

(Parker and Riches 1993). Dodders (Cuscuta spp.) arewidely distributed, being a threat to alfalfa (Medicagosativa L.), chickpea (Cicer arietinum L.), and lentil (Lensculinaris Medik.) in certain locations. The most importantspecies is Cuscuta campestris Yunck (Fig. 3).

There is no single technology to control these parasiticweeds (Joel et al. 2007; Parker 2009; Rubiales et al.2009b). Large areas of new territory are at risk of invasionif care is not taken to limit the introduction of parasiticweed seeds and to educate farmers and others to be on alertfor new infestations (Mohamed et al. 2006; Grenz andSauerborn 2007). The only way to cope with parasiticweeds is through an integrated approach, employing avariety of measures in a concerted manner, starting withcontainment and sanitation, direct and indirect measures toprevent the damage caused by the parasites, and finallyeradicating the parasite seedbank in soil.

2 Cultural practises

Preventing the movement of parasitic weed from infestedinto un-infested areas is a crucial component of control.Both sanitation and quarantine are required in order toprevent the dispersal of seeds. The minute seeds can easilybe transferred from one field to another by cultivation, andalso by water, wind, and animals. However, the mostsignificant seed transfer agents are people, transportationvehicles, and farming machines, which easily transfer seedsand contaminated soil. Once a field is infested withparasitic weeds, controlling its seed production is verydifficult. Extermination of seeds before their spread to newfields and regions is a crucial component in parasitic weedprevention program (Panetta and Lawes 2005). Quaternaryammonium salts have been found effective in seed

Fig. 1 Life cycle of parasiticweeds: on the left side, dodderseeds germinating, seedlingsattaching to close-by plants,climbing and growing andinfecting neighboring plants,flowering and setting seeds thatreplete the soil seed bank andrepeat the process; on the rightside, seeds of a weedy rootparasite (either Orobanche,Striga, or Alectra) germinating,attaching to the roosts of hostplants, emerging over the soilsurface, flowering and settingseeds that replete the soil seedbank and repeat the process

434 D. Rubiales, M. Fernández-Aparicio

eradication with complete seed kill achieved under com-mercial conditions at 0.5% a.i. of the disinfectant didecyldimethyl ammonium bromide.

Early plantings of cool season legumes are more severelyinfected by parasitic weeds. Delayed sowing is the best-documented traditional method for O. crenata avoidance(Rubiales et al. 2003b; Pérez-de-Luque et al. 2004b; Grenz etal. 2005). It also reduces S. gesnerioides (Touré et al. 1996)and dodder infection (Mishra et al. 2007). However, delayingsowing date implies shortening grain filling, which isdetrimental for yield. Thus, options are needed that combinethe yield benefit of early sowing with a decreased parasiticweed infestation.

Hand weeding can only be recommended in cases of limitedinfestation to prevent any further increase in the parasitepopulation and to reduce the seed bank in the soil. However,even when hand weeding is still commonly used in somecountries where no other feasible means of control are availableand the wages for labor are cheap, it is only practical inpreventing build-up of parasite seeds in slightly infested soils.

Solarization utilizes the sunlight in the summer toproduce high temperatures under clear polyethylene mulchthat covers the soil for several weeks. Mulching wet soilwith transparent polyethylene sheets for a period of 4–8 weeks during the warmest season proved to be effectivefor a number of vegetables but also for faba beans and lentil(Sauerborn et al. 1989a; Mauromicale et al. 2001).

Cultivation of the soil can strongly affect the parasiticweed seed bank. Minimum tillage can contribute toparasitic weed control by reducing the amount of viableseeds incorporated into the soil (Ghersa and Martínez-Ghersa 2000). No tillage has been reported to considerablyreduce O. crenata infection on faba bean (López-Bellido etal. 2009). On the other hand, deep-ploughing has beenrecommended to bring the seeds into a depth, where theycannot germinate due to the lack of oxygen (Van Delft et al.2000), but expectations have not been met sufficientlyperhaps due to problems with the costs and practicability.

Nitrogen compounds and manure fertilization has poten-tial for control of broomrape species. Nitrogen in ammo-

Fig. 3 Chickpea crop infectedby Orobanche crenata (A); byCuscuta campestris (B)

Fig. 2 Infection process of O. crenata on pea. A Germinating seedling contacting pea root; B haustorium formation resulting in tubercles; C budformation; D shoots starting to emerge; E flowering plants

Parasitic weeds management in legume crops 435

nium form affects negatively root parasitic weed germina-tion (Van Hezewijk and Verkleij 1996) and/or elongation ofthe seedling radicle (Westwood and Foy 1999). In addition,manure fertilization augments the killing effect of solariza-tion on O. crenata seeds (Haidar and Sidhamed 2000).

Intercropping is already used in Africa as a low-costmethod of controlling Striga hermonthica on cereals(Oswald et al. 2002). It has recently been shown thatintercrops with oat (Avena sativa L.) or with fenugreek(Trigonella foenum-graecum L.) or berseem clover (Trifo-lium alexandrinum L.) can reduce O. crenata infection onlegumes being allelopathy a major component for thereduction (Fernández-Aparicio et al. 2007, 2008b, c,2010a) (Fig. 4). The finding that germination of seedsexposed to synthetic germination stimulants is inhibited inpresence of oat or fenugreek roots suggest that oat rootsmight be exuding substances that inhibit O. crenata seedgermination. This has been confirmed in a subsequent work,and trigoxazonane identified from fenugreek (Evidente et al.2007) or benzoxazolinones (Fernández-Aparicio, unpub-lished) from oat root exudates that might be responsible forinhibition of O. crenata seed germination. Considerablegenetic variation in allelopathic activity has been foundwithin crops (Baghestani et al. 1999) which may allow forselection of more allelopathic cultivars.

Rotation may have direct and indirect impacts on parasiticweed in infested areas. While trap- and catch-crops in rotationmay reduce to some extent the parasite seed bank in soil, asdiscussed above, other rotation crops may have allelopathiceffects on parasitic weed seeds. Decreasing host croppingfrequency cannot, by itself, solve the parasitic weed problem.A nine-course rotation would be required to prevent O.crenata seedbank increases (Grenz et al. 2005).

The use of trap crops offers the advantage of stimulatingparasitic weed seed germination without being parasitized,

contributing to seed bank depletion. However, given thehigh amount of seeds in infested soils, it cannot be expectedthat the application of trap crops or germination stimulantswill eliminate the seed bank in the soil immediately. It is afeature of parasitic weeds that their numerous tiny seedsstay viable for a long time and never do germinate all at thesame time. The application of trap crops therefore shouldbe included in the regularly rotation and fallow manage-ment for the infested fields. For each species, suitable trapcrops need to be identified, as they show host specificity(Fernández-Aparicio et al. 2009a). For instance, pea is onlyinfected by O. crenata but pea root exudates stimulategermination of P. aegyptiaca, O. foetida, and O. minor(Fernández-Aparicio et al. 2008d) that are known to infectother legumes. Pea could be efficiently used as trap crop forthese species inducing suicidal broomrape germination.Other examples of potential trap crops are cereals such asdurum wheat (Triticum turgidum L.) and oat that stimulatedhigh germination of O. minor and P. aegyptiaca (Lins et al.2006; Fernández-Aparicio et al. 2009a) or sorghum(Sorghum bicolor (L.) Moench) that strongly stimulated S.gesnerioides (Berner and Williams 1998). The use ofcereals could be a suitable solution due to the highfrequency in which they are cultivated and its importancefor human consumption. For that reason, breeding on cerealgermplasm for the maximum inductor effect on broomrapeseeds could be of great interest. In fact clear genotypiceffects have been reported in sorghum in induction of S.gesnerioides germination (Berner and Williams 1998).Growing the selected varieties with high inductor potentialfor suicidal broomrape germination in rotations introducedin infected soils could shorten the time necessary betweenhost crops.

Catch crops in contrast to trap crops are plants which areheavily parasitized. Harvesting or destroying them after the

Fig. 4 Pea:oat intercrop reducing Orobanche crenata infectation in pea (A); detail of well-developed O. crenata seedlings when stimulated by pearoot exudates (B); restricted O. crenata seedling elongation by addition of L-tryptophan (C)


appearance of the parasite would dramatically reduce theseed potential in the soil. The ideal solution would be acatch crop of agronomical interest by itself.

There are claims of reduction in infestation in rotationswith rice due to water flooding (Sauerborn and Saxena1986); however, this has not been substantiated. It has alsobeen evidenced that soil irrigation during summer does notchange broomrape seed germination (López-Granados andGarcía-Torres 1996) what is in agreement with the highlevels of infection in faba bean in irrigated areas such as theNile Valley, quite often in rotations with rice.

3 Chemical control

3.1 Herbicides

The intimate connection between host and parasite also hindersefficient control by herbicides. Volatile compounds such asmethyl bromide, ethylene dibromide, metham-sodium, orformalin are effective for the control of broomrape (Foy et al.1989), but the high cost seldom justifies their use inlegumes. The herbicides that are currently in use forparasitic weed control are glyphosate, imidazolinones, orsulfonylureas (Joel et al. 2007). Glyphosate disrupts thebiosynthesis of aromatic amino acids inhibiting the keyenzyme 5-enolpyruvylshikimate-3-phosphate synthase(EPSPS), whereas imidazolinones and sulfonylurea herbi-cides inhibit acetolectate synthase (ALS) (Schloss 1995).All of them are systemic herbicides absorbed throughfoliage and roots of plants with rapid translocation to theattached parasite, which acts as a strong sink (Colquhounet al. 2006).

Chemical control of broomrape by foliar applications ofglyphosate at low rates is recommended for faba bean andvetches (Jacobsohn and Kelman 1980; Mesa-García andGarcía-Torres 1985; Sauerborn et al. 1989b), but problemsof lack of effectiveness or phytotoxicity can arise when it isnot applied properly. Selective control has also beenreported in lentils (Arjona-Berral and García-Torres 1983)at lower rates, but not in peas that are very sensitive toglyphosate. However, tolerance to glyphosate exists in peagermplasms that could be exploited in breeding (Sillero etal. 2001). Further, pea and other legumes could begenetically engineered with the glyphosate-resistance gene.

Pea and lentil tolerate better pre- and post-emergencetreatment of other herbicides suitable for broomrape controlsuch as imidazolinones (Jurado-Expósito et al. 1986).However, no complete control is provided, and treatmentis less effective in the earlier sowing dates (Rubiales et al.2003c) probably due to the dissipation of the herbicidefrom the sowing date till the time of broomrape establish-ment. Faba bean tolerates pre-emergence treatments of

imazapyr (12.5–25 g/ha) and imazethapyr (75–100 g/ha)and post-emergence treatments of imazapyr (2.5–5 g/ha),imazethapyr (20–40 g/ha), and imazaquin (40–60 g/ha)(García-Torres and López-Granados 1991). Lentil toleratespre-emergence treatments of imazapyr (25 g/ha) andimazethapyr (75 g/ha) and post-emergence treatments ofimazaquin (7.5 ml/ha) (Arjona-Berral et al. 1988; Jurado-Expósito et al. 1997) and imazapic (3 g/ha) (Bayaa et al.2000). Two post-emergence applications of imazapic arerecommended, with the first application recommendedwhen lentil has 5 to 7 true leaves, when broomrape usuallystarts to develop attachments on lentil roots, followed by asecond application 2 to 3 weeks later. Lentil may need athird application of 2 g/ha when late rain comes andextends the growth period, or when lentil is supplementaryirrigated (Bayaa et al. 2000). Phytotoxicity might be higherin the presence of water, low temperature, and heat stressesand vary with the lentil cultivar used (Hanson and Hill2001). An additional problem of these imidazolinoneherbicides for broomrape control is that they are notregistered in every country, and that doses and timing forapplication need to be adjusted case by case. Also,traditional imidazolinones are being replaced in somecountries by imazamox that has less residual in the soil,so doses and timing of application need re-adjustment.

Knowledge of the phenology of parasitic weeds isessential for their effective chemical control. Applicationmust be repeated in time interval of 2 to 4 weeks, becauseOrobanche seeds may germinate throughout the season andmay therefore re-establish on newly developed hosts roots.Models for broomrape development can be helpful forprecise chemical control. Such models, which exist for O.minor infecting red clover (Eizenberg et al. 2005) and as asubroutine of the Manschadi et al. (2001) model, can helpto anticipate the occurrence of parasite development stagessusceptible to, e.g., herbicide application. Advances inmodeling and the availability of new technologies areallowing the development of precision agriculture or site-specific farming. Parasitic weeds are usually distributed inpatches within the field (González-Andújar et al. 2001), soprecision agriculture techniques like discrimination by near-infrared reflectance spectroscopy (Jurado-Expósito et al.2003) could be adapted to detect broomrape-infected areasof the crop, for example, attending to differences intranspiration within infected and no infected plants.

Soil applications of sulfonylurea herbicides have proveneffective to control broomrape in tomato (Solanum lyco-persicum L.) and in potato (Solanum tuberosum L.), but theherbicide should be incorporated with irrigation. However,most cool season legume fields are not equipped withirrigation systems, because they are low input crops.Furthermore, legumes are not tolerant to sulfonylureaherbicides and probably will be injured when applied. For


such reasons, the only alternative should be pre-plantingapplication or post-planting incorporated with rainfall.

Seed treatments with imidazolinones have proven to beeffective controlling O. crenata in faba bean and lentil(Jurado-Expósito et al. 1997) and S. gesnerioides and A.vogelii in cowpea (Berner et al. 1994). The herbicide isincorporated as a coating on the seeds and distributedwith them at planting. This replaces a pre-emergencetreatment and saves mechanical application costs. Inaddition, it reduces the herbicide rate required by two- tothreefolds, being more environmental friendly. However,under favorable environmental conditions for broomrapeattack, the treatment must be supplemented to obtain highbroomrape control.

The efficient management of dodders starts with the useof dodder-free seed and the spraying of the first affectedpatches with a contact herbicide to prevent spread. Infestedequipment should be cleaned before and after use, and themovement of domestic animals from infested to dodder-freeareas should be limited. The application of pendimethalin at0.7–1.0 kg/ha as pre-emergence or early post-emergence iseffective against Cuscuta in lentil. In chickpea, Cuscuta isselectively controlled by pre-emergence application ofpropyzamide (0.5–0.75 kg/ha), pronamide (2.5 kg/ha), orpendimethalin (1.0 kg/ha) or by pre-sowing application ofWeedazol (Aminotriazol + ammonium thiocyanate) at 1.2–2.5 kg/ha. In faba bean, Cuscuta can be controlled withimazethapyr at 75 g/ha when applied pre-emergence or20 g/ha post-emergence (Khallida et al. 1993). In alfalfa,Cuscuta can be controlled by pre-emergence application ofimazethapyr at 0.1–0.15 kg/ha (Cudney and Lanini 2000)or pendimethalin (1.0 kg/ha) (Dawson 1990; Orloff et al.1989) or by post-emergence treatment with low doses ofglyphosate (0.075–0.15 kg/ha) (Dawson 1989).

Nanotechnology applications are already being exploredand used in medicine and pharmacology, but interest for usein crop protection is just starting. Nanoparticles can be usedas smart delivery systems for targeting and uploadingsubstances at specific areas within whole plants (González-Melendi et al. 2008; Corredor et al. 2009). The developmentof nanocapsules for controlled release and systemic applica-tion of herbicides will greatly increase the possibilities oftheir utilization against parasitic weed, for example, byallowing the use of herbicides with different modes of actionsuch as contact herbicides. The nanoparticles would carry theactive substance and specific property and/or externalmodification of these nanoparticles would allow theiraccumulation and/or guidance into broomrape-specific areasin which the chemical charge would be unloaded. Nano-encapsulation of herbicides could be used to solve problemsregarding phytotoxicity on the crop. Lower doses ofherbicides would be needed because they will not bedegraded by the crop, and they will accumulate preferentially

in the parasitic weed due to the sink effect (Pérez-de-Luqueand Rubiales 2009).

3.2 Suicidal germination

Orobanche, Phelipanche, Striga, and Alectra seeds requirechemical stimulation from the host root to germinate. Thissuggests that the artificial use of suitable chemicals mayreduce the parasitic weed seed bank by stimulating seedsgermination in the absence of a suitable host, which shouldlead to their demise due to their inability to survive withoutnutritional supply by a host. Attempts have been made withthe application to the soil of synthetic strigolactones, such asGR24 (Johnson et al. 1976) or Nijmegen-1 (Zwanenburg andThuring 1997). However, the application in the field has notyet been successful, due to the instability of the compound,particularly in alkaline soil, and probably also to the lack ofproper field application formulation for these compounds.

Several classes of plant secondary metabolites areknown to induce seed germination of root parasitic weeds(Yoneyama et al. 2008). More than ten strigol-relatedcompounds, collectively called strigolactones, have beenidentified as germination stimulants for root parasitic weeds(Yoneyama et al. 2009). Orobanchol, orobanchyl acetate,and 5-deoxystrigol are widely distributed in the Fabaceae(Yoneyama et al. 2008). Fabacyl acetate has recently beenidentified from root exudates of pea (Xie et al. 2009).Strigolactones play a major role in host specificity(Fernández-Aparicio et al. 2011). In addition to these, twonew compounds (peagol and peagoldione) have beenindentified in pea root exudates showing a selectivestimulation of Orobanche seed germination (Evidente etal. 2009). Successively, three polyphenols, named peapoly-phenols A–C, together with a polyphenol and a chalconewere isolated from same root exudates. Interestingly, onlypeapolyphenol A, 1,3,3-substituted propanone and 1,3-disubstituted propenone had specific stimulatory activityon O. foetida, not stimulating any other Orobanche orPhelipanche species tested (Evidente et al. 2010). Also, atriterpene and a sterol, identified as syasapogenol B andtrans-22-dehydrocampesterol, have recently been isolatedfrom common vetch root exudates. Soyasapogenol B wasvery specific stimulating germination of O. minor seedsonly, whereas trans-22-dehydrocampesterol stimulated P.aegyptiaca, O. crenata, O. foetida, and O. minor (Evidenteet al. 2011). Stimulatory activity of these metabolites onparasitic weed germination could be exploited in suicidalgermination control strategies by synthesizing and directlyapplying them to the field. Also, their production in plantscould be increased by breeding or by genetic transforma-tion. Soyasapogenol B increased has already been achievedin transgenic Medicago truncatula Gaertn. (Confalonieri etal. 2009).


Ethylene stimulates the germination of Striga andOrobanche seeds (Berner et al. 1999; Zehar et al. 2002).Other compounds of natural origin, such as fungalmetabolites (Fernández-Aparicio et al. 2008a), fungalphytotoxins, natural amino acids (Vurro et al. 2009), orplant or algae extracts (Economou et al. 2007) have alsobeen suggested for use in parasitic weed management,being able to inhibit seed germination or seedling elonga-tion, or, conversely, stimulate suicidal seed germination inthe absence of the host.

3.3 Activators of systemic acquired resistance

Systemic acquired resistance (SAR) has been reported in anumber of crops against different broomrape species byapplication of chemical agents (Sauerborn et al. 2002;Gonsior et al. 2004; Pérez-de-Luque et al. 2004a; Kusumotoet al. 2007). A significant reduction of O. crenata infectionin faba bean and pea was achieved under field conditions byfoliar application of BTH (1,2,3-benzothiadiazole-7-carbo-thioic acid S-methyl ester) (Pérez-de-Luque et al. 2004c). O.minor control has also been reported on red clover grown inplastic chambers after application of salicylic acid and BTHby inhibition elongation of O. minor radicles and theactivation of defense responses in the host root includinglignification of the endodermis (Kusumoto et al. 2007).Pérez-de-Luque et al. (2004a) described highly varyingsuccess on broomrape control after different BTH andsalicylic acid modes of application on pea in growth chamberexperiments. This shows that more host–parasite specificapplication techniques or perhaps other resistance inducingproducts are necessary to increase efficacy and reducenegative effects.

4 Biological control

Numerous microorganisms that might be useful for biocontrolof parasitic weeds have been isolated and reported (Amsellemet al. 2001; Boari and Vurro 2004; Sauerborn et al. 2007;Zermane et al. 2007). The fungal isolates reported to bepathogenic to parasitic weeds are for the most part Fusariumspp., prevailing especially strains of Fusarium oxysporumSchlecht.: Fr.. Advantages of Fusarium spp. relate to theirhost specificity and longevity in soil. However, to date, onlyF. oxysporum f. sp. orthoceras (Müller-Stöver et al. 2004)and F. solani (Mart.) Sacc. (Dor and Hershenhorn 2009) areunder investigation as potential candidates for broomrapecontrol. Ulocladium atrum (Preuss) Sacc. and Ulocladiumbotrytis Preuss have been found pathogenic towards O.crenata (Linke et al. 1992; Müller-Stöver and Kroschel2005). Myrothecium verrucaria (Alb. & Schwein.) Ditmarisolated from faba bean roots has been found to inhibit

germination of O. crenata seeds due to the production of themacrocyclic trichothecene, verrucarin A (El-Kassas et al.2005). Preliminary results demonstrated control of infectionof faba bean by O. crenata by the addition of spores of M.verrucaria to soil, raising the possibility that this approachmight be applicable in the field. Andolfi et al. (2005) isolatedseven macrocyclic trichothecenes, namely, verrucarins A, B,M, and L acetate, roridin A, isotrichoverrin B, and trichoverrolB from M. verrucaria and neosoloaniol monoacetate fromFusarium compactum was, a trichothecene, all being potentinhibitors of Pinguicula ramosa seed germination. Roridin Awas considered the metabolite with highest potential asherbicide, as at 1 μmol concentration, it preserves a highphytototoxic activity lacking zootoxicity (Andolfi et al.2005).

Some compatible Rhizobium strains have been reportedto decrease O. crenata infections in pea by activation ofoxidative process, LOX pathway, and production ofpossible toxic compounds, including phenolics and pisatin,inhibiting germination of O. crenata seeds, and causing abrowning reaction in germinated seeds (Mabrouk et al.2007). Colonization by the nitrogen-fixing bacteriumAzospirillum brasilense has also been reported to inhibitgermination and radicle growth of P. aegyptiaca (Dadon etal. 2004). Also colonization by arbuscular mycorrhizalfungi can provide protection against parasitic weeds asreported in cowpea reducing germination of S. gesnerioides(Lendzemo et al. 2009) or in pea reducing germination ofvarious Orobanche and Phelipanche species (Fernández-Aparicio et al. 2010b).

Most of the insects reported to occur on root parasiticweed species are polyphagous without any host specificityand thus, damage to these parasitic weeds is limited (Kleinand Kroschel 2002). However, for biological control, onlyoligo- and mono-phagous herbivorous insects are ofinterest. Smicronyx spp. has potential for Striga seedreduction (Kroschel et al. 1999). Phytomyza orobanchiaKalt. is a fly monophagous on broomrape. The feeding ofthe larvae within the capsules markedly diminishes seedmultiplication of the parasite (Klein and Kroschel 2002). P.orobanchia is widely distributed in the broomrape infectedarea, eating a substantial number of seeds (Rubiales et al.2001). This natural infestation is however insufficient toreduce broomrape in areas with heavy broomrape infesta-tions. Nevertheless, bio-control with P. orobanchia can behelpful to slow down further dissemination and infestationin weakly infested areas and can be part of an integratedcontrol approach to reduce the seed bank in heavily infestedsoils. This effect could be substantially increased bymassive propagation and inundative release of this insect(Klein and Kroschel 2002).

Further success of mycoherbicides in agricultural appli-cations will depend largely on the development of an


appropriate formulation which allows storage, handling,and a successful application of the fungal propagules(Shabana et al. 2003; Sauerborn et al. 2007). Effectivenessof biological control could be increased by the combinationof two or more pathogens (Charudattan 2001). For instance,F. oxysporum f. sp. orthoceras and F. solani gave a lowcontrol Orobanche cumana in sunflower (Helianthusannuus L.) when used individually, but when applied as amixture control improved (Dor et al. 2003). Integration ofSAR inducers with F. oxysporum f. sp. orthoceras alsoresulted in highly reliable control of O. cumana (Müller-Stöver et al. 2005). The engineering of hypervirulencegenes into weed-specific pathogens is receiving increasingattention (Gressel et al. 2004).

Another potential strategy would be to change the enduses, so that broomrape would be a desirable product in itsown right. In the Puglia region of Italy, O. crenata isconsidered a tasty vegetable very appreciated by consumers.There are several recipes for cooking broomrape that areoffered in restaurants (Rubiales 1999). Alternative uses mightinclude the pharmaceutical and cosmetic industries (Andary1993).

5 Resistance breeding

5.1 Breeding for resistance to the parasites

Breeding for disease resistance is straight-forward when agood source of resistance is available and an efficient,easily controlled, and practical screening procedure existsto provide good selection pressure. Unfortunately, this isnot the case in legumes against broomrape (Rubiales 2003;Rubiales et al. 2006). The only instance in whichbroomrape resistance of simple inheritance has beenidentified and widely exploited in breeding is in sunfloweragainst O. cumana Wallr. This has been particularlyimportant allowing a rapid progress in sunflower breedingagainst O. cumana (Fernández-Martínez et al. 2008). O.crenata resistance identified in legumes so far is ofpolygenic nature (Román et al. 2002a; Valderrama et al.2004; Fondevilla et al. 2010). Faba bean breeding for O.crenata resistance was founded using the Egyptian lineF402 as source of resistance (Nassib et al. 1982). Similarly,resistance against O. foetida has also been identified in fababean germplasm. Some lines selected against O. crenatahave also shown a high level of resistance to O. foetida,with a high yield potential (Abbes et al. 2007).

Little resistance is available within pea germplasmagainst O. crenata (Rubiales et al. 2003c), but promisingsources of resistance have been identified in wild relativeswithin the genus Pisum (Rubiales et al. 2005a; Pérez-de-Luque et al. 2005a), which have successfully been

hybridized with cultivated pea (Rubiales et al. 2009a).Resistance is also very limited in grass pea (Lathyrussativus L.) and chickling vetch (Lathyrus cicera L.)(Fernández-Aparicio et al. 2009b; Fernández-Aparicio andRubiales 2010), but is available in related Lathyrus species(Sillero et al. 2005a). Resistance in lentils has only recentlybeen reported (Fernández-Aparicio et al. 2008e, 2009c).However, resistance is frequent in common vetch andchickpea germplasm and cultivars (Gil et al. 1987; Rubialeset al. 2003a; Fernández-Aparicio et al. 2008f) as well as intheir wild relatives (Rubiales et al. 2004, 2005a; Sillero etal. 2005b). Resistance to P. aegyptiaca has been found inpurple vetch (Vicia atropurpurea Desf.) (Goldwasser et al.1997) (Fig. 7).

Cowpea breeding for resistance to S. gesnerioides inWest Africa was founded using the Botswana landraceB301 as a source of resistance. Following extensive fieldevaluation, a number of new resistant cultivars have beenreleased. Different dominant genes for resistance have beenidentified in lines resistant to different S. gesnerioidesstrains identified in West Africa so these have been used ascomplimentary parents when breeding for all strains (Singh2002; Timko et al. 2007). Resistance to Alectra wasdiscovered after screening more than 650 cowpea acces-sions. Landraces B301 and B359 appeared to be particu-larly useful (Riches 1987, 1989). It is important to noticethat landrace B301 is resistant to both S. gesnerioides andA. voguelii, being resistance to each weed conferred byindependent non-allelic genes (Atokple et al. 1993).

5.2 Pathogenic variation

Knowledge on the existence of host specialization andparasite races is vital for any breeding program. There is noclear evidence for the existence of races of O. crenata.Molecular analysis suggest that most of the intraspecificvariation in O. crenata is among individuals and not amonghosts nor between regions (Román et al. 2002a) whatsupports the lack of physiological races and the high flowamong broomrape populations. Only several levels of host-driven differentiation have been described in O. minorgrowing on Trifolium pratense and Daucus carota ssp.gumminfer (Thorogood et al. 2009) or O. foetida onchickpea and faba bean (Román et al. 2007). Races havenot been described in any of these species and the lack ofselection pressure by the host due to the lack of highlyresistant cultivars to any of these species. It would appear atleast possible that new parasitic biotypes could originate,however, as O. crenata populations are very heterogeneous(Román et al. 2001, 2002b). There is the risk that diverseO. crenata populations could be selected for virulencewhen challenged by the widespread use of highly resistantcultivars. In fact, a new race of O. crenata has been


suggested in Israel attacking resistant vetches (Joel 2000).This putative race seems to have been selected by thefrequent culture of the resistant vetch cultivar in the area.

There is considerable variation in host specificity betweenisolates of S. gesnerioides, and different host species vary intheir susceptibility to different parasite isolates. Mohamed etal. (2001) described eight Striga host-specific strains calledEuphorbia, Ipomoea, Indigofera, Jaquemontia, Merremia,Nicotiana, Tephrosia, and Vigna strains. The Vigna strain isby far the most important, causing considerable damage tocowpea. It was initially proposed that there are five distinctraces of S. gesnerioides in West and Central Africa, based ontheir ability to differentially parasitize different cowpea lines(Lane et al. 1997). At least seven distinct races wererecognized in a later study with genome profiling withmolecular markers and host differential resistance response(Botanga and Timko 2006). Because of the autogamousnature of S. gesnerioides, variations among isolates becomegenetically fixed, and geographic distributions of morpho-types, strains, and races frequently overlap (Parker andRiches 1993).

Although less systematic research has been completedwith A. vogelii, it is clear that there is also variability in thevirulence of populations of this parasite in different areas ofAfrica (Riches et al. 1992). A. vogelii also has distinct racesthat differentially parasitize cowpea (Polniaszek et al.1991).

5.3 Resistance mechanisms

Resistance against root parasitic weeds is a multicomponentevent, being the result of a battery of avoidance factors and/or resistance mechanisms acting at different levels of theinfection process (Joel et al. 2007; Pérez-de-Luque et al.2008, 2009; Rubiales et al. 2009a). Avoidance due toprecocity is known in some legumes, early floweringgenotypes having an advantage limiting O. crenata infection(Rubiales et al. 2005a; Fernández-Aparicio et al. 2009b)(Fig. 5) what can be explained by an earlier pod-setting andmaturity, which would restrict the dry-matter partitioning intoparasites (Grenz et al. 2005).

Some pre-attachment mechanisms of resistance could beacting prior to parasite contact with the host root. One ofthem is low induction of seed germination. It has beensuccessfully used in sorghum breeding for resistance to S.hermonthica (Ejeta 2007) but has not been identified inlegumes against S. gesnerioides. Resistance to O. crenataassociated to low induction of parasite seeds germinationhas been reported in several legumes (Pérez-de-Luque et al.2005a; Rubiales et al. 2003a, 2004; Sillero et al. 2005).Another pre-attachment mechanism could be related to thechemotropism responsible for the correct guidance of thebroomrape seedling towards the host root. A wrongorientation of germinated O. crenata seeds within thepotentially infective distance has been observed in pea(Pérez-de-Luque et al. 2005a) (Fig. 6) probably due tochanges in the concentration of compounds exuded fromhost roots that are responsible for the chemotropic responseof the seedlings (Whitney and Carsten 1981). Pre-haustorialmechanisms of resistance consisting in physical barrierssuch as protein crosslinking, callose depositions, andsuberization reinforcing cortical cell walls (Pérez-de-Luqueet al. 2006a, 2007) or in lignification of endodermal cells(Pérez-de-Luque et al. 2005b, 2007) have also beenidentified in legumes. In addition, chemical barriers in theform of accumulation and excretion of phytoalexins into theapoplast have been identified in the central cylinder of M.truncatula (Lozano-Baena et al. 2007).

Post-haustorial resistance mechanims, where attachedparasites fail to develop, have also been described in legumes.These can be physical response consisting on sealing of hostvessels by gel or gum-like substances and blocking the flux ofwater and nutrients from the host to the parasite (Pérez-de-Luque et al. 2005b, 2006b) or chemical, consisting ondelivery of toxic compounds such as phenolics into the hostvascular system causing death of O. crenata tubercles onchickpea (Pérez-de-Luque et al. 2006c) and M. truncatula(Lozano-Baena et al. 2007) or of P. aegyptiaca in purplevetch (Goldwasser et al. 1999) (Fig. 7).

A rapid necrosis of the host cells around the point ofinfection, leading to the death of the parasite, has also beenidentified in cowpea against S. gesnerioides (Lane et al.

Fig. 5 Effects of earliness onOrobanche crenata infection: Avery early Lathyrus accessionfilling pods and escaping fromO. crenata infection; B lateaccession heavily infected


1993). Another resistance mechanism was observed inother cowpea cultivars consisting in growth arrest of S.gesnerioides tubercles. Although tubercles began to developon the host root surface, they did not enlarge, remaining lessthan 0.5 mm in diameter or their cotyledons failed to expand(Lane and Bailey 1992; Lane et al. 1993).

Resistance to Cuscuta has only recently been reported inchickpea characterized by the failure of the prehaustoriumto penetrate the chickpea stem (Goldwasser et al. 2009).

5.4 Potential use of molecular markers and biotechnologiesin resistance breeding

The development of marker-assisted selection (MAS) techni-ques for broad-based polygenic resistance is a particularlypromising approach since parasitic weed resistance tests aredifficult, expensive, and sometimes unreliable.

In pea, quantitative trait loci (QTLs) conferring resistanceto O. crenata have been identified (Valderrama et al. 2004;Fondevilla et al. 2010). However, QTLs identified explaineda low portion of the observed variation (altogether 21%). Anin vitro screening method assaying different phases of theparasite cycle using a Petri dish technique, enabled identifi-cation of QTLs governing specific mechanisms of resistance,explaining a higher proportion of the variation (38–59%,depending on the trait) (Fondevilla et al. 2010).

In faba bean, three QTLs linked to resistance wereidentified in a map developed using an F2 populationsegregating for the trait (Román et al. 2002b). The QTLsexplained a high percentage of the phenotypic variation ofthe trait (74%), mainly because of one of the QTL Oc1,which explained more than 37% of the character. Unfortu-nately, when a RIL population derived from this same crosswas evaluated in other seasons and locations, this QTLvanished (Díaz-Ruiz et al. 2010), showing that it was not astable QTL and should therefore be excluded for MAS.Two additional QTLs for resistance against O. foetida wereidentified using the same RIL, but both instable acrossenvironments and explained very little phenotypic variation(7–9%) (Díaz-Ruiz et al. 2009). The accuracy of pheno-typic evaluation is of the utmost importance for theaccuracy of QTL mapping. These screenings for broomraperesistance were performed under field conditions with notsufficient control of crucial environmental factors and ofhomogeneity of inoculum in the soil. Also, assessmentswere based on final number of emerged broomrapes perplant in the infested fields, what is likely to be influence bymany confounding factors (Fernández-Aparicio et al.2009b) such as earliness or plant vigor (Fondevilla et al.2010). These can be avoidance to the contact by reduced rootbiomass or root architecture, low induction of broomrape seedgermination, resistance to penetration, and/or hampered

Fig. 6 Successful Orobanchecrenata infection on pea in mini-rhizotrons (A) versus failedPhelipanche aegyptiaca attemps(B): seeds germinated, but failedto infect due to a combinationof wrong orientation of radiclesand arrested root penetration

Fig. 7 Successful (A) versusfailed (B) penetration of Pheli-panche aegyptiaca in roots oftwo different vetch genotypes(Mezquita vs. Popany). Picturestaken 11 days after parasiticradicle contacted with thehost root


development of established tubercles (Rubiales et al. 2006;Pérez-de-Luque et al. 2010). To overcome the disadvantagesof screenings under field conditions, phenotyping should beperformed using mini-rhizotrons, allowing the dissection ofthe resistance into specific mechanisms acting in differentstages of the infection process, increasing the accuracy of theassessment, as done in pea (Fondevilla et al. 2010).

The genetic basis of resistance to S. gesnerioides and A.vogelii parasitism has been examined by a few laboratories.Single genes conferring resistance to S. gesnerioides(named Rsg genes: Touré et al. 1997; Ouédraogo et al.2001; Li et al. 2009) or to A. vogelii (named Rav genes:Atokple et al. 1993, 1995) have been reported. Molecularmarkers linked to Rsg1-1, Rsg2-1, Rsg3-1, Rsg4-3, andRsg994-1 genes for S. gesnerioides resistance have beenidentified, and several sequence-confirmed amplifiedregions have been developed for use in marker-assistedselection (Ouédraogo et al. 2002; Li et al. 2009). Markerslinked to A. vogelii resistances are being sought (Kouakouet al. 2009).

Although QTLs for resistance to O. crenata have beenidentified in pea and faba bean, they cannot yet be used inMAS. Saturation of genomic regions associated withbroomrape resistance is needed to facilitate the identifica-tion of the most tightly linked markers that could be used totransfer the genes/QTLs responsible to the broomrape. Thedistances between the flanking markers and QTLs are stillhigh and numerous recombinants between the QTL flankingmarkers and resistance are expected. Therefore, before usingthe available QTLs in MAS, the genomic regions containingthe QTLs should be further saturated in order to refine theposition of the QTLs and to identify molecular markers moreclosely linked to the resistance genes. The identification of thegenes governing resistance included in the QTLs would allowthe development of primers for these genes. These primerswould be really useful for MAS, as they would be specific andrecombination between the markers and resistance would beabsent.

Novel strategies for the control of plant pathogens includeselective silencing of target genes by small interfering RNAs(siRNA) (Prins et al. 2008). A key component to success withRNAi technology is identifying the best parasite genes tosilence (Yoder et al. 2009). Sequence information obtainedfrom different parasite species can be used to clone thehomologous gene from a particular pest or can be directlytransformed into crop plants.

5.5 Lessons to learn from model legumes

The use of model plants is valuable to identify newresistance genes that can be directly transferred or reintro-duced under the control of a more active promoter viagenetic transformation to improve resistance in crops.

Following the example of other plant pathogen–interaction,the use of model plants such as Arabidopsis thaliana (L.)Heynh., M. truncatula, Lotus japonicus L., and rice (Oryzasativa L.), may improve our understanding of the plant–parasitic plant interaction. A. thaliana and M. truncatula aresuitable hosts of some Orobanche species (Westwood 2000;Rodríguez-Conde et al. 2004; Fernández-Aparicio et al.2008d), while rice may be used to study Striga (Gurney etal. 2006). L. japonicus can be infected by P. aegyptiaca butshows incompatible interaction against O. minor and S.gesnerioides (Kubo et al. 2009). Further studies should thustake advantage of these models to get insight more rapidlyinto the molecular bases of plant resistance, which shouldimprove the efficiency of both MAS and transgenicapproaches for crop improvement toward resistance toparasitic plants. The powerful “omics” tools implementedfor M. truncatula makes this species highly suitable as amodel for these studies (Dita et al. 2006, 2009; Die et al.2007; Rispail et al. 2007, 2010; Castillejo et al. 2009).

M. truncatula is resistant to O. crenata, with ratherinsufficient variation in resistance among accessions ham-pering its use for genetic studies and presenting a non-hostrather than host resistance response (Fernández-Aparicio etal. 2008d; Lozano-Baena et al. 2007). However, otherOrobanche species different from O. crenata, might infectM. truncatula. Significant variation in the level of resistance/susceptibility to O. aegyptiaca, O. foetida, P. nana (Reut.)Soják and P. ramosa (L.) Pomel is available in M. truncatulagermplasm (Fernández-Aparicio et al. 2008d). Genomicresources developed in M. truncatula (Young and Udvardi2009) have the potential to accelerate practical advances incrop legumes.

Gene expression studies provide another source ofcandidate genes for parasitic weed resistance. They allowincreasing the knowledge on the molecular basis of theresistance and the mechanisms underlying the host–parasiteinteraction. To improve our understanding of the M.truncatula–O. crenata, a suppression subtractive hybridiza-tion (SSH) library was created allowing the identification ofcandidate genes for O. crenata defense (Die et al. 2007). Inaddition, a microarray analysis of the M. truncatula genesregulated in response to O. crenata has been performed ona M16kOLI1 microarray platform (Dita et al. 2009). Theseanalyses revealed the activation of both the salicylic acid(SA) and jasmonate defense pathways. Hybridization of M.truncatula microarray chips with RNA from related speciessuch as pea is possible (Fondevilla et al. 2011). Thus, thesame microarray platform may eventually be used directlywith RNA from pea, allowing a more comprehensiveunderstanding of pea molecular response to broomrape.

Differential expression studies in cowpea suggested thatPR5 expression may be a useful marker of S. gesneroidesinfection, and that salicylic acid signaling appears to play a


role in the cowpea–S. gesnerioides interaction (Li et al.2009). Resistance to S. gesnerioides has been knockeddown by virus-induced gene silencing (Li and Timko2009). The differential display approach has also beenapplied to Cuscuta-infected alfalfa, showing the inductionof PR genes such as PPRG2, a PR-10 homolog (Borsicsand Lados 2002), and a calmodulin-related protein, PPRG1,indicating that defense signaling pathways to dodder islinked to calcium (Borsics and Lados 2001).

A proteomic approach was also applied to compare theproteome of two pea genotypes differing in their sensitivity toO. crenata at different stages of the infection (Castillejo et al.2004). However, only 25% of the proteins differentiallyregulated were identified by mass spectrometry, hampered bythe low number of pea sequences available in databases. Theuse of M. truncatula allowed the identification of moreproteins involved (Castillejo et al. 2009).

5.6 Breeding for resistance to the herbicides

Herbicide-treated crops with target-site resistances wouldallow control of parasitic weeds (Gressel 2009). Theherbicide would pass through the plant and flow into thehidden parasite; it is essential for this mode of action thatthe host plant does not metabolize the herbicide. In targetsite resistance, the parasite takes the herbicide together withthe nutrients from the protected host and thereby accumu-lates toxic levels. This hypothesis has been already borneout by using transgenic crops with target-site resistance forthe acetolactate synthase (ALS), enolphosphate shikimatephosphate (EPSP) synthase, and dihydropteroate synthase-inhibiting herbicides allowing control of Striga or Oro-banche (Gressel 2009). This is therefore, a promisingsolution for controlling parasitic weeds in legumes. Resis-tance could be transferred into legumes following existingprotocols, allowing an efficient broomrape control. How-ever, apart from the difficulties of transforming legumeplants, other drawbacks such as high cost, lengthydevelopment time, and high economic risk, limit the useof this solution (Duke and Cerdeira 2005).

Imidazolinone-tolerant plants with altered ALS genesand enzymes have been discovered in many crops throughmutagenesis and selection. This allowed developing byconventional breeding methods of imidazolinone-tolerantmaize, wheat, sorghum, rice, oilseed (Brassica napus L.),and sunflower (Tan et al. 2004). Imidazolinone-tolerantmutations have also been discovered in other crops, and itis technically possible to identify them in legume crops anddevelop imidazolinone-tolerant cultivars by breeding. Anumber of lentil cultivars are being introduced to themarket under the trademark “CLEARFIELD® lentils”(BASF Agsolutions 2008) that are not genetically modifiedand that tolerate higher doses of imidazolinone herbicides.

However, ALS-inhibitor resistance can rapidly evolve inweeds as a consequence of repeated application of herbicideswith this site of action. In fact, resistance to ALS inhibitorherbicides such as chlorsulfuron and sulfometuron-methyl hasalready been reported in C. campestris (Rubin 1994).Herbicide mixtures are recommended to manage herbicideresistance.

6 Conclusions

In this review, we discuss the most advanced methods forparasitic weed control in legumes. Some of these methodsare ready for commercial use by farmers (chemical control),some are in the final stages of development towardcommercialization (resistant varieties and sanitation), andsome need further development and improvement beforecommercial implementation (biological control).

Altogether, the available control methods have not provento be as effective, economical, and applicable as desired.Although several potential control measures were developedin the past decades for some crops, any approach appliedalone is often only partially effective and sometimes incon-sistent and affected by environmental conditions.

The only way to cope with the parasitic weeds is throughan integrated approach, employing a variety of measures ina concerted manner, starting with containment and sanita-tion, direct and indirect measures to prevent the damagecaused by the parasites, and finally eradicating the parasiteseedbank in soil. Much research is needed in order todevelop new means for parasitic weed control. Basicresearch should provide new targets for control within thelife cycle of the parasites and among their metabolicactivities. The genomic research of parasitic weeds, whichhas already started, is likely to help in an overall understandingof some key aspects of parasitism.

Acknowledgments Support by project AGL2008-01239 isacknowledged.

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